Abstract
The anatomically simple plants that first colonized land must have acquired molecular and biochemical adaptations to drought stress. Abscisic acid (ABA) coordinates responses leading to desiccation tolerance in all land plants. We identified ABA nonresponsive mutants in the model bryophyte Physcomitrella patens and genotyped a segregating population to map and identify the ABA NON-RESPONSIVE (ANR) gene encoding a modular protein kinase comprising an N-terminal PAS domain, a central EDR domain, and a C-terminal MAPKKK-like domain. anr mutants fail to accumulate dehydration tolerance-associated gene products in response to drought, ABA, or osmotic stress and do not acquire ABA-dependent desiccation tolerance. The crystal structure of the PAS domain, determined to 1.7-Å resolution, shows a conserved PAS-fold that dimerizes through a weak dimerization interface. Targeted mutagenesis of a conserved tryptophan residue within the PAS domain generates plants with ABA nonresponsive growth and strongly attenuated ABA-responsive gene expression, whereas deleting this domain retains a fully ABA-responsive phenotype. ANR orthologs are found in early-diverging land plant lineages and aquatic algae but are absent from more recently diverged vascular plants. We propose that ANR genes represent an ancestral adaptation that enabled drought stress survival of the first terrestrial colonizers but were lost during land plant evolution.
Highlights
Plants successfully colonized terrestrial habitats ;500 million years ago and changed the face of the planet (Kenrick and Crane, 1997; Kenrick et al, 2012; Wickett et al, 2014)
The response to abscisic acid (ABA) is achieved through a highly conserved core signaling pathway, in which a family of receptor proteins bind ABA, which potentiates a molecular interaction with protein phosphatase 2C (PP2C) enzymes
When P. patens protoplasts or protonemal explants are regenerated in the presence of ABA, the cells exhibit a characteristic change in growth habit characterized by cellular differentiation producing brachycytes—small, round, thick-walled, nonvacuolate cells in which vacuolation and cell expansion is suppressed (Figure 1)—interspersed with tmema cells (Decker et al, 2006)
Summary
Plants successfully colonized terrestrial habitats ;500 million years ago and changed the face of the planet (Kenrick and Crane, 1997; Kenrick et al, 2012; Wickett et al, 2014). The response to ABA is achieved through a highly conserved core signaling pathway, in which a family of receptor proteins (the PYRABACTIN RESISTANCE1 [PYR1]/PYR1-LIKE [PYL]/REGULATORY COMPONENTS OF ABA RECEPTORS [RCAR] proteins) bind ABA, which potentiates a molecular interaction with protein phosphatase 2C (PP2C) enzymes (e.g., those encoded by the ABSCISIC ACID INSENSITIVE1 [ABI1] and ABI2 genes) Sequestration of these phosphatases by the ABAbound receptors allows the phosphorylation of SnRK2 protein kinases that in turn activate phosphorylation of transcription factors (e.g., the ABI5 bZip transcription factor) that trigger ABAmediated transcription of the genes encoding dehydration tolerance-associated proteins (Park et al, 2009; Cutler et al, 2010)
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